Diptera: Chironomidae) in the Alaskan Arctic
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CHIRONOMUS Journal of Chironomidae Research No. 33, 2020: 48-58. Current Research. EVIDENCE OF PARTHENOGENETIC POPULATIONS FROM THE PARATANYTARSUS LACCOPHILUS SPECIES GROUP (DIPTERA: CHIRONOMIDAE) IN THE ALASKAN ARCTIC Alec R. Lackmann1,2, Daniel C. McEwen3, Malcolm G. Butler4 1University of Minnesota Duluth, Department of Biology, 1035 Kirby Drive, SSB 207, Duluth, MN 55812. 2North Dakota State University, Department of Biological Sciences, Environmental and Conservation Sci- ences Program, PO Box 6050, Fargo, North Dakota, USA 58108. E-mail: [email protected] 3Limnopro Aquatic Science, Inc. PO Box 764, St. Cloud, MN 56302. E-mail: [email protected] 4North Dakota State University, Department of Biological Sciences, Fargo, North Dakota, USA. E-mail: [email protected] Abstract Introduction Parthenogenesis, reproduction without fertiliza- While sexual reproduction is widespread in the tion, is not common in the Chironomidae (Dip- animal kingdom, parthenogenesis is a widespread tera), a family of insects with more than 6,000 form of asexual reproduction in which there is no described species. Nonetheless, parthenogenetic fertilization of the egg (Suomalainen 1962; Lynch species and strains have been documented in at 1984). Parthenogenesis in animals evolves most least three subfamilies (the Chironominae, Or- commonly as an artifact of hybridization (Carew et thocladiinae, and Telmatogoninae), spanning 17 al. 2013) and is most often thelytokous, i.e. where genera and ~30 species. One such species, Para- all asexually produced offspring are female. Be- tanytarsus laccophilus Edwards 1929, is known to cause offspring are genetically monotonous with be parthenogenetic in a small portion of its range mutation as the only source of variation (Lynch in Finland, with most other European populations 1984), parthenogenesis is often considered an evo- of this species showing evidence of sexual repro- lutionary dead end (Darlington 1946; Mayr 1970; duction. We present evidence of parthenogenetic Smith 1978). Nonetheless, patterns exist in the populations from the Paratanytarsus laccophilus distribution of parthenogenetic forms that suggest species group in the Nearctic, specifically a High this reproductive strategy could be evolutionarily Arctic site near Utqiaġvik (formerly Barrow), advantageous in certain cases. Alaska. During May-July of 2015 and 2016, we “Geographic parthenogenesis” describes the ob- sampled emerging adult chironomids and pupal servation that parthenogenesis tends to evolve exuviae daily to document insect emergence phe- in habitats that are different from where their nologies. Across 15 local populations, all 623 pu- closely related, sexually-reproducing relatives re- pal exuviae collected from the P. laccophilus spe- side (Vandel 1928). Indeed, parthenogenetic spe- cies group were female. Larvae reared from two cies are most commonly documented from high populations under controlled temperature treat- latitudes, especially in harsh habitat conditions ments emerged as female adults (N=37). When (Lynch 1984). Proposals articulated to account for isolated, these reared female adults oviposited, and this phenomenon include the “biotic-uncertain- eggs hatched successfully. These progeny were ty” hypothesis (Ghiselin 1974), and the “tangled reared for another 12-13 days, reaching second bank” hypothesis (Bell 1982). The biotic-uncer- instar larvae when they were preserved at the end tainty hypothesis postulates that parthenogens tend of our field season. Taken together, this evidence to persist in harsh environments that are relatively strongly indicates parthenogenesis from the P. lac- barren biologically, and an environment with mini- cophilus species group at this location. This spe- mal biotic interaction favors the persistence of ge- cies was not previously documented at Utqiaġvik. netically monotonous lineages. The tangled bank Although parthenogenetic, their emergence at this hypothesis argues that harsh environments are location was highly synchronized. In the harsh en- less niche-specialized because they are frequently vironment of arctic Alaska, the fitness rewards of disturbed. This selects against genetically diverse parthenogenesis are likely great. Indeed, chirono- progeny pre-adapted to fill a diverse array of nich- mid parthenogenesis in the northern hemisphere es, providing opportunities for clonal populations. is most commonly documented from far-northern These rather intuitive hypotheses include many as- extremes and in extreme habitats. sumptions, remain untested, and are unsatisfactory in explaining geographic parthenogenesis (Lynch 1984). 48 Although parthenogenesis is rather widespread Of the at least 6,434 described chironomid spe- across some insect groups such as the Hymenop- cies to date (ISC 2017; Stur and Ekrem 2020), less tera (Suomalainen 1962), it is relatively uncom- than 0.5% (~30 species) are known as partheno- mon in the Chironomidae (Lindeberg 1951; Armit- gens (Table 1). These represent 3 of the 11 extant age et al. 1995; Gokhman and Kuznetsova 2017). chironomid subfamilies (Cranston et al. 2012): the These non-biting midge flies are often the most Chironominae, Orthocladiinae, and Telmatogoni- common and species-rich macroinvertebrate taxon nae. In the Chironominae, there are 17 partheno- in freshwater habitats, with estimates of the total genetic species found among 7 genera (Grimm richness of this family surpassing 10,000 species 1870; Thienemann 1954; Lindeberg 1958; Linde- (Armitage et al. 1995), with the tropics still poorly berg 1971; Grodhaus 1971; Oliver and Danks studied (Ferrington 2007). 1972; Armitage et al. 1995; Langton 1998; Donato and Paggi 2008; Porter and Martin 2011); in the Table 1. Chironomid taxa with evidence of parthenogenesis as of 2020. Subfamily Taxon Reference Chironominae Tanytarsus norvegicus (Kieffer, 1924) Lindeberg 1971 Tanytarsus gregarius (Kieffer, 1909) Lindeberg 1971 Tanytarsus sp. (sylvaticus) Lindeberg 1971 Tanytarsus sp. (lestagei) Lindeberg 1971 Tanytarsus heliomesonyctios (Langton, 1999) Langton 1998 Paratanytarsus grimmii (Schneider, 1885) Grimm 1870 Paratanytarsus laccophilus (Edwards, 1929) Lindeberg 1958 Paratanytarsus sp. (boiemicus) Lindeberg 1971 Micropsectra silvesterae (Langton, 1999) Langton 1998 Micropsectra sp. (nigripila) Armitage et al. 1995 Micropsectra sedna (Oliver, 1976) Porter et al. 2011 Chironomus atrella (Townes, 1945) Grodhaus 1971 Chironomus attenuatus (Walker, 1848) Grodhaus 1971 Chironomus stigmaterus (Say, 1823) Grodhaus 1971 Lauterborniella sp. Oliver et al. 1972 Polypedilum parthenogeneticum (Donato and Paggi, 2008) Donato et al. 2008 Zavreliella marmorata (Wulp, 1858) Thienemann 1954 Orthocladiinae Corynoneura celeripes (Winnertz, 1852) Edwards 1919 Corynoneura donovani (Forsyth, 1971) Forsyth 1971 Corynoneura scutellata (Winnertz, 1846) Edward et al. 1968 Limnophyes minimus (Meigen, 1818) Armitage et al. 1995 Limnophyes vestitus (Skuse, 1889) Forsyth 1971 Abiskomyia virgo (Edwards, 1937) Armitage et al. 1995 Bryophaenocladius furcatus (Kieffer, 1916) Armitage et al. 1995 Eretmoptera murphyi (Schaeffer, 1914) Armitage et al. 1995 Metriocnemus abdominoflavatus (Picado, 1913) Thienemann 1954 Phytotelmatocladius delarosai (Epler, 2010) Siri et al. 2014 Pseudosmittia baueri (Strenzke, 1960) Armitage et al. 1995 Troglocladius hajdi (Andersen, Baranov et Hagenlund, 2016) Andersen et al. 2016 Telmatogetoninae Telmatogeton amphibious (Eaton, 1875) Crafford 1971 Telmatogeton sp. Delettre et al. 2003 49 Orthocladiinae there are 12 species from 9 genera identifying female midges, parthenogenesis in the (Edwards 1919; Thienemann 1954; Edward and Chironomidae may be more common than previ- Colless 1968; Forsyth 1971; Armitage et al. 1995; ously believed (Ekrem et al. 2010; Stur and Ekrem Siri and Donato 2014; Andersen et al. 2016; Bart- 2020). lett et al. 2018); and in the Telmatogetoninae there Not only do parthenogenetic chironomids vary in are two species from the type genus Telmatogeton habitat, but they also vary in the extent of their (Crafford 1971; Delettre et al. 2003). parthenogenesis. Some of the taxa in Table 1 are Of all these parthenogenetic species (Table 1), strictly parthenogenetic, like Paratanytarsus grim- the best represented genera are Tanytarsus, Para- mii, the globally-distributed, notorious pest of tanytarsus, Micropsectra, Corynoneura, and Lim- water-supply systems (Carew et al. 2013). Other nophyes, while at the other extreme some genera taxa (e.g. Tanytarsus heliomesonyctios) exhibit show very limited evidence of parthenogenesis population-specific parthenogenesis, with parthe- (e.g. Chironomus) (Oliver and Danks 1972; Armit- nogenesis evident for populations that occur in age et al. 1995). Although most parthenogenetic relatively harsh environmental conditions (Orel chironomids are found in arctic and subarctic and Semenchenko 2019; Stur and Ekrem 2020). habitats (Armitage et al. 1995), others are reported This is also the case for Paratanytarsus laccophi- from sub-Antarctic islands (Crafford 1971; Delet- lus. Lindeberg (1958, 1971) documented parthe- tre et al. 2003), phytotelmata in Argentina (Siri et nogenetic populations of P. laccophilus in rock al. 2014), and a cave in Croatia (Andersen et al. pools on the isles of the Gulf of Finland, yet found 2016). Furthermore, since many of these parthe- bisexual reproduction in all other locations where nogenetic chironomids are triploid and of hybrid he studied this species. Here we present evidence origin, they are permanent genetic heterozygotes